Bacterial spot disease, a complex of four Xanthomonas species, is among the most widespread and destructive diseases of tomatoes and peppers throughout the world, causing lesions on aerial plant parts leading to defoliation and fruit loss [1]. It has chronically afflicted U.S. tomato production, particularly in Florida, where the largest production of fresh market tomatoes occurs. Ninety-seven percent of Florida acres are affected, and yield losses may reach fifty percent of marketable production [2].
Various crop protection compounds have been used to control bacterial spot in commercial tomato and pepper production. In the 1950s, streptomycin was commonly used to control plant diseases caused by bacteria, including bacterial spot. Xanthomonas euvesicatoria (Race T1), the prevalent bacterial spot race in Florida at the time, quickly became resistant to streptomycin [3], [4], and its use was discontinued. In the 1960s, fixed copper compounds and copper-fungicide mixes became the primary means of bacterial spot control. Initially fixed copper was used alone, but resistance in xanthomonads developed quickly [5]. In response to observing increased efficacy when copper was mixed with ethylenebisdithiocarbamate (EBDC) fungicides such as maneb and mancozeb, growers began mixing fixed copper products with EBDC fungicides for improved bacterial spot control [5]. However, even these copper-fungicide mixes have become ineffective against tomato races of the pathogen, especially under conditions of high humidity and warm temperatures that favor heavy disease pressure (eg [6], [7], [8], [9]; Table 4).
Because crop protection compounds do not control the copper tolerant Xanthomonas races responsible for this disease, genetic resistance against bacterial spot has been a priority in tomato breeding programs. These breeding efforts have been slowed by the complex genetics of resistance and changing races of the pathogen, and consequently there are no commercial varieties with effective resistance to Xanthomonas. One commonly bred form of plant disease resistance relies on the evolution of specific intracellular immune receptors encoded by disease resistance, or R, genes. R genes have been selected through conventional breeding for over 100 years [10]. They encode specific receptors that recognize gene products made by specific races of a given pathogen species. These pathogen components are termed effectors, and they contribute to pathogen virulence by suppressing or modulating host defenses in susceptible plant genotypes that lack a corresponding R gene [11].
AvrBs2 is an effector that is highly conserved in a number of Xanthomonas species that infect a wide range of plant hosts, including tomato [12]. Unlike other key effectors, it is present in all six races of the tomato bacterial spot disease complex (Table 5). Mutations in AvrBs2 can impair virulence, indicating that it plays an important role in pathogenicity and may be a good target for durable resistance [12].
AvrBs2 is recognized by the R protein Bs2, identified in pepper, a fellow member of the Solanaceae and close relative of tomato. Previously, transgenic tomato plants expressing the Bs2 gene were reported to have enhanced resistance to bacterial spot disease following vacuum infiltration of leaves with Xanthomonas campestris pv. vesicatoria (Xcv) in the laboratory [13]. However, at that time resistance was not assessed under field conditions nor with the prevalent Xanthomonas strains that are known to cause bacterial spot disease of tomato.